Pulmonary involvement in Sjögren’s syndrome | Medicina Clínica (English Edition)

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(A) Cutaneous manifestations of a patient with dermatomyositis and anti-MDA5 antibodies: ulcers and digital papules (left and right, arrows). (B) Initial HRCT scan (left image) of a patient with ILD and anti-MDA5 antibodies that shows subpleural reticulation associated with minimal ground glass areas and some traction bronchiectasis (arrow). Control HRCT of the same patient at 2 years (right image), with a significant worsening compared to the previous HRCT. 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El desafío continúa" ] ] "contieneTextoCompleto" => array:1 [ "en" => true ] "contienePdf" => array:1 [ "en" => true ] "autores" => array:1 [ 0 => array:2 [ "autoresLista" => "Vicente Boix, Esperanza Merino" "autores" => array:2 [ 0 => array:2 [ "nombre" => "Vicente" "apellidos" => "Boix" ] 1 => array:2 [ "nombre" => "Esperanza" "apellidos" => "Merino" ] ] ] ] ] "idiomaDefecto" => "en" "Traduccion" => array:1 [ "es" => array:9 [ "pii" => "S0025775321006072" "doi" => "10.1016/j.medcli.2021.10.002" "estado" => "S300" "subdocumento" => "" "abierto" => array:3 [ "ES" => false "ES2" => false "LATM" => false ] "gratuito" => false "lecturas" => array:1 [ "total" => 0 ] "idiomaDefecto" => "es" "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S0025775321006072?idApp=UINPBA00004N" ] ] "EPUB" => "https://multimedia.elsevier.es/PublicationsMultimediaV1/item/epub/S2387020622000468?idApp=UINPBA00004N" "url" => "/23870206/0000015800000004/v1_202202170636/S2387020622000468/v1_202202170636/en/main.assets" ] "en" => array:19 [ "idiomaDefecto" => true "cabecera" => "Review" "titulo" => "Pulmonary involvement in Sjögren’s syndrome" "tieneTextoCompleto" => true "paginas" => array:1 [ 0 => array:2 [ "paginaInicial" => "181" "paginaFinal" => "185" ] ] "autores" => array:1 [ 0 => array:4 [ "autoresLista" => "Jaume Mestre-Torres, Roser Solans-Laque" "autores" => array:2 [ 0 => array:4 [ "nombre" => "Jaume" "apellidos" => "Mestre-Torres" "email" => array:1 [ 0 => "jmestre@vhebron.net" ] "referencia" => array:3 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] 1 => array:3 [ "nombre" => "Roser" "apellidos" => "Solans-Laque" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] ] ] ] "afiliaciones" => array:2 [ 0 => array:3 [ "entidad" => "Unidad de Enfermedades Autoinmunes Sistémicas, Servicio de Medicina Interna, Hospital Vall d‘Hebron, Barcelona, Spain" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Departamento de Medicina, Facultad de Medicina, Universidad Autónoma de Barcelona, Barcelona, Spain" "etiqueta" => "b" "identificador" => "aff0010" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Síndrome de Sjögren y afectación pulmonar" ] ] "textoCompleto" => "IntroductionSjögren’s syndrome (SS) is a systemic autoimmune disease characterised by the presence of exocrine glandular hypofunction, predominantly ocular and oral, expressed as xerophthalmia (dry eyes) and xerostomia (dry mouth). However, SS can affect multiple organs<a class="elsevierStyleCrossRefs" href="#bib0005">1,2</a> and the extraglandular or systemic involvement is what determines the prognosis of the disease. Immunologically, SS is characterised by the presence of antinuclear antibodies (ANA) with a speckled immunofluorescence pattern, and anti-Ro60 and/or anti-Ro52, and anti-La antibodies. Other antibodies associated with SS are rheumatoid factor (RF), present in 50% of cases, and anti-centromere antibodies, present in 3%–27% of cases.<a class="elsevierStyleCrossRef" href="#bib0015">3</a> The criteria for the classification of SS have varied over the last decades. Currently they include the demonstration of a decrease in salivary and tear secretion, and the presence of positive immunology (anti-Ro60 antibodies) and/or a focal lymphocytic infiltrate in the salivary glands, forming accumulations of more than 50 lymphocytes.<a class="elsevierStyleCrossRef" href="#bib0005">1</a> Although the extraglandular involvement is what determines the prognosis, it has not been included in the different classification criteria.An index of disease activity has been developed, the EULAR Sjögren’s syndrome disease activity index (ESSDAI), which assesses 12 different domains (glandular, joint, pulmonary, neurological, haematological, etc.). It is defined as low-grade activity when a patient has <5 points on the ESSDAI score, moderate between 5 and 13 points, and high-grade when 14 or more points are obtained.<a class="elsevierStyleCrossRef" href="#bib0020">4</a>SS can affect the bronchial respiratory system with the occurrence of bronchiectasis and/or with involvement of the pulmonary interstitium. Interstitial involvement can develop in the form of usual interstitial pneumonia (UIP), non-specific interstitial pneumonia (NSIP) or lymphoid pneumonitis, among others.<a class="elsevierStyleCrossRef" href="#bib0025">5</a> The exact incidence of SS-associated lung involvement is not known,<a class="elsevierStyleCrossRef" href="#bib0030">6</a> although it is estimated to be present in 15%–35% of patients.Respiratory symptoms related to Sjögren’s syndromeJS-related respiratory symptoms are varied, very often non-specific and usually develop progressively during disease follow-up, although they may be present at the time of diagnosis.<a class="elsevierStyleCrossRef" href="#bib0035">7</a> Clinically, patients report dry cough, xerotrachea and symptoms compatible with bronchial hyperresponsiveness. In addition, they may present with recurrent respiratory infections and dyspnoea. It is not uncommon for these symptoms to precede the diagnosis of the disease and go unnoticed.<a class="elsevierStyleCrossRef" href="#bib0040">8</a> Systematic examination of the respiratory system is therefore important. The prevalence of dry cough and xerotrachea, defined as the persistent sensation of dryness in the pharyngeal and retrosternal area, is 40%–50%.<a class="elsevierStyleCrossRef" href="#bib0045">9</a> Other less common symptoms are anosmia, nasal crusts and nosebleed due to nasal dryness.<a class="elsevierStyleCrossRefs" href="#bib0050">10,11</a> Airway involvement may appear in the form of bronchiectasis or bronchial hyperresponsiveness and is associated with an increased frequency of respiratory infections. The prevalence of bronchiectasis can be up to 10%.<a class="elsevierStyleCrossRef" href="#bib0060">12</a>The development of interstitial lung disease (ILD) is more common in older patients and in those with Raynaud’s phenomenon and gastrointestinal involvement in the form of motility disorder and gastroesophageal reflux.<a class="elsevierStyleCrossRef" href="#bib0040">8</a> Its presence is not associated with specific clinical manifestations, although progressive dyspnoea is its main symptom.Immunology and diagnosis of Sjögren’s syndromeAs already mentioned, most patients with SS are ANA positive and approximately 50% are RF positive. However, the 2016 classification criteria for SS only include anti-Ro-60/SSA antibodies, which are present in 60%–70% of cases.<a class="elsevierStyleCrossRef" href="#bib0005">1</a> Although anti-Ro/SSA antigen is known to comprise two subunits (Ro60 and Ro52), many laboratory techniques cannot differentiate one subunit from another.<a class="elsevierStyleCrossRef" href="#bib0065">13</a> Anti-Ro52 antibodies are not considered diagnostic of SS.<a class="elsevierStyleCrossRef" href="#bib0070">14</a> Therefore, although in an appropriate clinical context the presence of anti-Ro52 is suggestive of SS, it should be borne in mind that it is of a more non-specific nature and can be found in various systemic autoimmune diseases such as systemic lupus erythematosus, scleroderma or rheumatoid arthritis, where its presence is associated with Raynaud’s phenomenon and/or interstitial lung disease.<a class="elsevierStyleCrossRefs" href="#bib0075">15–18</a> Similarly, the finding of hypergammaglobulinemia, positive ANA or RF results in a patient with sicca syndrome does not allow the patient to be classified as having SS.<a class="elsevierStyleCrossRef" href="#bib0095">19</a> Thus, if positive ANA, RF, or anti-Ro52 results are detected, a complete history-taking and physical examination should be performed to assess the possible presence of an autoimmune disease<a class="elsevierStyleCrossRef" href="#bib0075">15</a> and, if SS is suspected, a minor salivary gland biopsy should be performed to confirm the diagnosis. In fact, the histopathological study of the minor salivary gland is usually diagnostic in 37%–50% of patients with sicca syndrome, ANA and/or RF but negative for anti-Ro60/SSA antibodies.Regarding immunological findings, the presence of anti-centromere antibodies (ACA), typically associated with scleroderma, has been described in up to 20% of patients with SS, although it seems that these antibodies would recognize a different epitope.<a class="elsevierStyleCrossRef" href="#bib0015">3</a> If present, therefore, an overlap between the two diseases must be ruled out, especially if there is interstitial lung involvement.<a class="elsevierStyleCrossRef" href="#bib0100">20</a>Diagnosis of patients with SS who do not have anti-Ro60 is often more complex, as minor salivary gland biopsy is not always diagnostic. Nevertheless, the clinician should use all available options to achieve such a diagnosis, as extraglandular complications can occur with similar severity in anti-Ro60 positive and anti-Ro60 negative patients and may be the initial manifestation of the disease.<a class="elsevierStyleCrossRef" href="#bib0105">21</a> In these patients, it is especially important to perform a minor salivary gland biopsy, which would confirm the diagnosis and its classification, or other tests such as parotid gland ultrasound, salivary scintigraphy and a complete assessment of tear function, which can reinforce the suspected diagnosis.<a class="elsevierStyleCrossRef" href="#bib0110">22</a>Clinical-radiological diagnostic evaluation of lung involvementCharacterization of pulmonary involvement in SS should be done in a multimodal way, evaluating clinical manifestations, respiratory function tests (RFTs) and radiological findings on chest high-resolution computed tomography (HRCT).Pulmonary function tests should include a complete spirometry, including lung volumes with a bronchodilator test and the diffusing capacity of lung for CO test (DLCO). These tests will allow us to screen for the presence of airway and/or parenchymal pathology,<a class="elsevierStyleCrossRef" href="#bib0145">29</a> as well as detect significant changes that may lead to the initiation of immunosuppressive or antifibrotic treatment during disease progression.<a class="elsevierStyleCrossRef" href="#bib0150">30</a> In addition, they will allow us to rule out the possible existence of pulmonary arterial hypertension.<a class="elsevierStyleCrossRef" href="#bib0155">31</a> Patients with SS may exhibit alterations in pulmonary function tests, both obstructive and restrictive. If a restrictive pattern and/or a decrease in DLCO is found, parenchymal or vascular involvement in the lungs should be considered.<a class="elsevierStyleCrossRef" href="#bib0160">32</a> In patients with obstructive lung involvement, whether or not associated with restrictive compromise, consideration should be given to possible airway involvement.<a class="elsevierStyleCrossRef" href="#bib0145">29</a>Radiologically, the gold standard for the study of the airway and lung parenchyma is a chest HRCT, which should include an expiratory phase study to assess the presence of air trapping. The most commonly observed findings are a combination of ground glass opacities, consolidations, honeycombing, cross-linking, and the occurrence of cysts, nodules, and bronchiectasis,<a class="elsevierStyleCrossRef" href="#bib0165">33</a> with the NSIP pattern being the most common in terms of interstitial involvement.<a class="elsevierStyleCrossRef" href="#bib0040">8</a> The study by Roca et al.<a class="elsevierStyleCrossRef" href="#bib0105">21</a> found such involvement in 33.3% of patients, followed by the UIP pattern (23.8%), lymphoid interstitial pneumonia (9.5%) and organising pneumonia (9.5%). 23.8% of patients had an indeterminate pattern on HRCT. The possible existence of an underlying lymphoma should be assessed in any patient presenting with lymphoid interstitial pneumonia, pulmonary cysts or nodules and a suggestive clinical context (cytopenias, C4 hypocomplementemia, presence of rheumatoid factor or monoclonal gammopathy).<a class="elsevierStyleCrossRefs" href="#bib0170">34–36</a> It is noteworthy that, unlike in scleroderma, the EULAR guidelines for the management of SS do not assess the extent of interstitial involvement on chest HRCT to justify changes in treatment, although symptoms and functional lung involvement do.<a class="elsevierStyleCrossRefs" href="#bib0185">37,38</a>The prevalence of bronchiectasis in SS is not well defined, with a variable proportion between 7%–54%<a class="elsevierStyleCrossRef" href="#bib0025">5</a> having been reported. Bronchiectasis is usually cylindrical and predominantly occurs in the lower lobes of the lungs. These findings have been associated with a higher frequency of hiatal hernia and an increased risk of respiratory infections.<a class="elsevierStyleCrossRef" href="#bib0025">5</a>Consensus recommendations from The Sjögren’s Foundation (USA) have recently been published describing the pulmonary evaluation of patients with JS with and without known pulmonary involvement.<a class="elsevierStyleCrossRef" href="#bib0160">32</a> These recommendations can be differentiated according to the presence of airway and/or interstitial involvement. In patients without respiratory symptoms, a chest X-ray and RFTs are recommended as a baseline evaluation. Routine chest HRCT is not recommended. Rather, a chest HRCT and RFTs should be performed in patients with respiratory symptoms. As there is insufficient evidence, there is no established frequency for follow-up imaging or RFTs, and it is recommended that follow-up be done on an individual basis. Routine bronchoscopy with bronchoalveolar lavage or transbronchial biopsy is not recommended for the diagnosis of interstitial involvement.Finally, according to the ESSDAI index, SS activity in the lungs is classified as absent, mild, moderate or severe/intense, depending on the findings in the complementary diagnostic tests and the patient’s symptoms (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). Tests that define the severity of pulmonary involvement include RFTs and chest HRCT. Other diagnostic tests used for respiratory evaluation include the six-minute walk test, lung ultrasound, or chest MRI. ESSDAI considers chronic damage to be those symptoms, findings on chest HRCT or RFTs, which do not change over 12 months.<a class="elsevierStyleCrossRef" href="#bib0190">38</a> Thus, despite the abnormality in the examinations, if there is no change in the previous 12 months, these findings score zero on the ESSDAI index.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>Pulmonary histopathology and Sjögren’s syndromeThe most characteristic finding of pulmonary interstitium histology in SS is the combination of several pathological patterns. The most commonly found pattern is NSIP, described in up to 45% of lung biopsies from patients with SS, showing interstitial inflammation with varying degrees of fibrosis in a lung with preserved architecture.<a class="elsevierStyleCrossRef" href="#bib0025">5</a> The second histological pattern by frequency is UIP, present in between 16%–33% of patients with ILD and SS. Histological manifestations are characterized by honeycombing, patchy fibrosis with isolated fibroblastic foci, and mild interstitial inflammation along with patchy alveolar infiltrates of lymphocytes, plasma cells, and lymphoid follicles with germinal centres.<a class="elsevierStyleCrossRef" href="#bib0060">12</a> Lymphoid interstitial pneumonia is characterized by a diffuse lymphoid infiltrate. These lymphocytes are polyclonal and are accompanied by plasma cells, occasionally forming lymphoid follicles and even germinal centres.<a class="elsevierStyleCrossRef" href="#bib0060">12</a> The possible existence of bronchus-associated lymphoid tissue (BALT) lymphoma should be taken into account in patients with interstitial involvement and SS, considering that this may be low-grade and the morphological findings difficult to characterize.<a class="elsevierStyleCrossRef" href="#bib0195">39</a>The study of other respiratory areas is also important. Mononuclear cell infiltration of the airway has been demonstrated in the trachea, bronchi and bronchioles and may affect the exocrine glands in this region.<a class="elsevierStyleCrossRef" href="#bib0200">40</a> In addition, bronchoalveolar lavage studies have also shown a CD4+ T lymphocyte predominance, even in asymptomatic patients.<a class="elsevierStyleCrossRef" href="#bib0025">5</a>Lymphoma and lung involvementSS-associated lymphomas are usually mucosa-associated lymphoid tissue (MALT) type. Radiographic findings on chest HRCT are in the form of pulmonary nodules or areas of consolidation, often indistinguishable from benign processes or lymphocytic pneumonia.<a class="elsevierStyleCrossRefs" href="#bib0170">34,41</a> The use of PET/CT in the event of a clinical suspicion can be useful for its diagnosis when the patient reports B symptoms, constitutional symptoms, etc.,<a class="elsevierStyleCrossRef" href="#bib0210">42</a> as it is non-specific. The clinical and laboratory factors most commonly associated with lymphoma are parotid gland enlargement, cryoglobulinaemic vasculitis, leukopenia (<3000 cells/mm3), positive La immunology and C4 hypocomplementemia. It has been shown that the higher the number of risk factors, the higher the positive predictive value for lymphoma, so the finding of such markers should alert us to this possibility.<a class="elsevierStyleCrossRefs" href="#bib0175">35,43</a>Differential diagnosis of pulmonary involvement in Sjögren’s syndromeILDs are a group of entities that have in common the inflammatory and fibrosing involvement of the lung parenchyma.<a class="elsevierStyleCrossRef" href="#bib0135">27</a> Primary pulmonary diseases and interstitial diseases associated with systemic diseases have been described. For this reason, it is recommended that its evaluation be carried out in a multidisciplinary manner, including clinicians, radiologists and pathologists.<a class="elsevierStyleCrossRef" href="#bib0140">28</a>In recent years, a new entity called interstitial pneumonia with autoimmune features (IPAF) has been defined but, in reality, it should be considered as a working diagnosis and not an entity per se.<a class="elsevierStyleCrossRef" href="#bib0115">23</a> A diagnosis of IPAF is considered in patients with ILD of unknown aetiology, with clinical and serological findings or thoracic morphological changes suggestive of an underlying autoimmune disease, but who cannot be diagnosed with any of them.In the case of a patient with IPAF, it is important to perform a thorough history-taking and physical examination since these will allow us to classify the patient in some cases. If SS is suspected, a complete ophthalmological evaluation (Schirmer’s test, tear break-up time and corneal staining) should be performed to rule out dry eye, and salivary secretion should be assessed by salivary flow quantification or salivary scintigraphy, and a minor salivary gland biopsy should be considered if the diagnosis of SS is still suspected but cannot be confirmed, as they do not have specific anti-Ro60<a class="elsevierStyleCrossRefs" href="#bib0120">24,25</a> antibodies. It should be noted that sicca syndrome was not included in the definition of IPAF as it is not very specific and that anti-Ro52 and anti-Ro60<a class="elsevierStyleCrossRef" href="#bib0130">26</a> antibodies were not differentiated immunologically.Therefore, it is of particular interest to consider the possibility of SS in patients with interstitial lung involvement of non-infiltrative aetiology, who present associated sicca syndrome, even if they do not have specific immunology.Treatment and lung involvement in Sjögren’s syndromeGuidelines published by the European League Against Rheumatism (EULAR) in 2019 recommend multidisciplinary assessment of patients with SS. These recommendations were made through the evaluation of studies published up to 2017 using a Delphi process, with no evidence of significant progress in recent years. Treatment is mainly based on symptomatic control of the sicca syndrome, glucocorticoids and immunosuppressants.<a class="elsevierStyleCrossRef" href="#bib0220">44</a>The consensus guidelines of The Sjögren’s Foundation recommend treatment according to the site of the pathology, airway or pulmonary interstitium, and according to the severity of symptoms, severity of organ involvement and treatment progression. These include symptomatic treatment, glucocorticoids, immunosuppressants, biological therapy, and antifibrotic agents.<a class="elsevierStyleCrossRef" href="#bib0160">32</a> Some authors have described that they use different treatments depending on the chest HRCT findings.<a class="elsevierStyleCrossRef" href="#bib0125">25</a> However, although it is known that different radiological patterns are associated with different prognosis, no specific treatment guidelines have been described as the current evidence is scarce.<a class="elsevierStyleCrossRefs" href="#bib0025">5,29,45</a>Regarding SS-related pulmonary involvement, the 2019 EULAR guidelines recommend a treatment adjusted to the clinical findings and the ESSDAI score. Inhaled therapy is recommended in patients with bronchial involvement and systemic treatment when there is ILD. If involvement is moderate, glucocorticoid monotherapy is recommended, and if activity is high, glucocorticoid treatment followed by oral immunosuppression is proposed. Glucocorticoids should be used at the lowest possible dose and for the shortest possible time to avoid side effects. No immunosuppressive drug is prioritised but reports in the published literature suggest the more widespread use of azathioprine, mycophenolate or cyclosporine A. Intravenous pulsed cyclophosphamide or rituximab<a class="elsevierStyleCrossRef" href="#bib0220">44</a> are proposed as rescue therapy. Retrospective series of patients with SS or connective tissue diseases (including SS) have shown that azathioprine, mycophenolate or rituximab are associated with improved pulmonary function tests, with fewer complications than oral cyclophosphamide.<a class="elsevierStyleCrossRefs" href="#bib0105">21,46,47</a> Rituximab has also shown encouraging results, although with an increased risk of respiratory infections.<a class="elsevierStyleCrossRef" href="#bib0240">48</a> Despite these findings, there are no randomized clinical trials comparing these treatments, so the recommendations are not robust.Antifibrotic therapy has shown promising results in patients with progressive fibrosing lung diseases. The INBUILD clinical trial demonstrated a reduction in the annual fall in forced vital capacity in such patients, including 170 participants (25.6% of the total cohort) with systemic autoimmune diseases.<a class="elsevierStyleCrossRef" href="#bib0245">49</a> Systemic diseases in this group included rheumatoid arthritis, scleroderma, Sjögren’s syndrome, mixed connective tissue disease, undifferentiated connective tissue disease and IPAF. A post-hoc analysis of this cohort showed that in this subgroup of patients the effect of nintedanib was maintained.<a class="elsevierStyleCrossRef" href="#bib0250">50</a> It should be noted that specific studies have not been performed in patients with SS unlike other systemic autoimmune diseases such as scleroderma.<a class="elsevierStyleCrossRef" href="#bib0185">37</a>If, despite drug therapy, there is a progression of the disease with a decline in lung function and a deterioration in quality of life, patients should be evaluated by lung transplant teams. There is no consensus regarding the indication for transplantation given the limited evidence available and the presence of contradictory results. On the one hand, a retrospective study in which patients with ILD related to connective tissue diseases were compared with patients with idiopathic pulmonary fibrosis, showed that the clinical course was similar in both groups. This progression was studied in relation to survival, acute or chronic rejection and/or existence of extrapulmonary dysfunction. In this cohort, patients with scleroderma were excluded, but a total of 26 patients with Sjögren’s syndrome were included (9.5% of the total cohort).<a class="elsevierStyleCrossRef" href="#bib0255">51</a> On the other hand, a Spanish cohort including 26 patients (4 of them with SJS) showed a trend towards shorter survival in patients with connective tissue disease compared to those with idiopathic pulmonary fibrosis.<a class="elsevierStyleCrossRef" href="#bib0260">52</a> Thus, more studies are needed to evaluate the indication for lung transplantation in the context of SS.The treatment protocol carried out in our center includes bronchodilator therapy for patients with predominantly obstructive airway involvement. Patients with interstitial lung disease were initiated on prednisone at medium doses (0.5 mg/kg bw/day), with a progressive decrease in dose to 5 mg/day, together with mycophenolate at progressive doses up to 720 mg/12 h. If the patient has bronchiectasis, azathioprine (1−2 mg/kg bw/day) is prioritised over mycophenolate, given the risk of respiratory infections associated with the use of this drug in this group of patients. In patients with progressive lung disease despite immunosuppressive therapy, treatment with rituximab is initiated. Patients with progressive fibrosing ILD are started on antifibrotic therapy with nintedanib.ConclusionsPulmonary disease in SS is an understudied entity and often underdiagnosed in routine clinical practice, as it presents with non-specific symptoms. In all patients diagnosed with SS, the presence of respiratory symptoms should be investigated and an extensive work-up by physical examination and additional tests should be performed when there is suspicion of both interstitial and airway involvement. Further studies are needed to define a specific pulmonary treatment for this disease, based on the extent of the disease and co-existence with other systemic conditions.FundingThis article has been prepared without funding.Conflict of interestsThe authors declare that they have no conflicts of interest in relation to the authorship and/or publication of this article." "textoCompletoSecciones" => array:1 [ "secciones" => array:16 [ 0 => array:3 [ "identificador" => "xres1666601" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1480849" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1666602" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1480848" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:2 [ "identificador" => "sec0010" "titulo" => "Respiratory symptoms related to Sjögren’s syndrome" ] 6 => array:2 [ "identificador" => "sec0015" "titulo" => "Immunology and diagnosis of Sjögren’s syndrome" ] 7 => array:2 [ "identificador" => "sec0020" "titulo" => "Clinical-radiological diagnostic evaluation of lung involvement" ] 8 => array:2 [ "identificador" => "sec0025" "titulo" => "Pulmonary histopathology and Sjögren’s syndrome" ] 9 => array:2 [ "identificador" => "sec0030" "titulo" => "Lymphoma and lung involvement" ] 10 => array:2 [ "identificador" => "sec0035" "titulo" => "Differential diagnosis of pulmonary involvement in Sjögren’s syndrome" ] 11 => array:2 [ "identificador" => "sec0040" "titulo" => "Treatment and lung involvement in Sjögren’s syndrome" ] 12 => array:2 [ "identificador" => "sec0045" "titulo" => "Conclusions" ] 13 => array:2 [ "identificador" => "sec0050" "titulo" => "Funding" ] 14 => array:2 [ "identificador" => "sec0055" "titulo" => "Conflict of interests" ] 15 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2021-04-07" "fechaAceptado" => "2021-06-01" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1480849" "palabras" => array:3 [ 0 => "Sjögren’s síndrome" 1 => "Intersitial lung disease" 2 => "Sicca syndrome" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1480848" "palabras" => array:3 [ 0 => "Síndrome de Sjögren" 1 => "Enfermedad pulmonar intersticial" 2 => "Síndrome seco" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Sjögren’s syndrome is an autoimmune disease that involves exocrine glands. The most characteristic symptoms consist of the sicca syndrome (including xerostomia and dry eye - xerophtalmia), but can involve multiple organs. The extraglandular involvement determines the prognosis. It is tipically associated with the presence of antinuclear antibodies, including Ro-60 antibodies. Pulmonary involvement appears as bronchiectasis and/or interstitial pneumonia. Considering its high prevalence, it must be ruled out in all patients with respiratory symptoms by performing pulmonary function tests and high resolution computed tomography of the chest. Evaluation can be completed with a transbronchial biopsy if diagnostic doubts persist. Treatment includes steroid therapy, inmunosupressive or antifibrotic drugs, or biological therapy. In selected cases pulmonary transplantation must be considered." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "El síndrome de Sjögren es una enfermedad autoinmune que afecta a las glándulas exocrinas. Su sintomatología característica es el síndrome seco en forma de xeroftalmia y xerostomía, pero puede afectar a diversos órganos o sistemas, y la afectación extraglandular es la que condiciona el pronóstico de la enfermedad. Típicamente se asocia con la presencia de anticuerpos antinucleares, que incluyen anti-Ro-60. La afectación pulmonar aparece en forma de bronquiectasias y/o neumopatía intersticial. Dada la alta prevalencia de esta complicación, su presencia debe descartarse en todos los pacientes con síntomas respiratorios mediante pruebas de función respiratoria y tomografía computarizada de alta resolución torácica. Se puede completar la valoración mediante biopsia transbronquial en aquellos casos en que existan dudas diagnósticas. El tratamiento incluye glucocorticoterapia, terapia inmunosupresora o antifibrótica, y terapia biológica. En caso de mala evolución se debe valorar el trasplante pulmonar." ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "Please cite this article as: Mestre-Torres J, Solans-Laque R. Síndrome de Sjögren y afectación pulmonar. Med Clin (Barc). 2022;158:181–185." ] ] "multimedia" => array:1 [ 0 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0005" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "ESSDAI: EULAR Sjögren’s syndrome disease activity index; NYHA: New York Heart Association; RFTs: respiratory function tests; Chest HRCT: Chest high-resolution computed tomography; DLCO: diffusing capacity of lung for CO; FVC: Forced vital capacity." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Activity level \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Description \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Without activity \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">No active lung involvement. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Mild \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Persistent cough secondary to bronchial involvement. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Pulmonary involvement should be ruled out by chest HRCT and RFTs. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">The patient cannot have dyspnoea. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Moderate \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Evidence of interstitial lung disease by chest HRCT. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">RFTs abnormalities: 70% > DLCO ≥ 40% or 80% > FVC ≥ 60%. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">There may be dyspnoea on exertion with a NYHA functional class II. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">High \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Evidence of interstitial lung disease with dyspnoea NYHA functional class III-IV. \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">RFTs abnormalities: DLCO < 40% or FVC < 60%. \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2837378.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Classification of pulmonary signs and symptoms according to the Sjogren’s syndrome activity index (ESSDAI) of the European League Against Rheumatism (EULAR)." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:52 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "2016 American College of Rheumatology/European League Against Rheumatism classification criteria for primary Sjögren’s syndrome: a consensus and data-driven methodology involving three international patient cohorts" "autores" => array:1 [ 0 => array:2 [ "etal" => true "autores" => array:6 [ 0 => "C.H. 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Pulmonary involvement in Sjögren’s syndrome

Síndrome de Sjögren y afectación pulmonar

Jaume Mestre-Torresa,b,

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jmestre@vhebron.net

Corresponding author.

, Roser Solans-Laquea,b

a Unidad de Enfermedades Autoinmunes Sistémicas, Servicio de Medicina Interna, Hospital Vall d‘Hebron, Barcelona, Spain

b Departamento de Medicina, Facultad de Medicina, Universidad Autónoma de Barcelona, Barcelona, Spain

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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Sj&#246;gren&#8217;s syndrome &#40;SS&#41; is a systemic autoimmune disease characterised by the presence of exocrine glandular hypofunction&#44; predominantly ocular and oral&#44; expressed as xerophthalmia &#40;dry eyes&#41; and xerostomia &#40;dry mouth&#41;&#46; However&#44; SS can affect multiple organs<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;2</span></a> and the extraglandular or systemic involvement is what determines the prognosis of the disease&#46; Immunologically&#44; SS is characterised by the presence of antinuclear antibodies &#40;ANA&#41; with a speckled immunofluorescence pattern&#44; and anti-Ro60 and&#47;or anti-Ro52&#44; and anti-La antibodies&#46; Other antibodies associated with SS are rheumatoid factor &#40;RF&#41;&#44; present in 50&#37; of cases&#44; and anti-centromere antibodies&#44; present in 3&#37;&#8211;27&#37; of cases&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> The criteria for the classification of SS have varied over the last decades&#46; Currently they include the demonstration of a decrease in salivary and tear secretion&#44; and the presence of positive immunology &#40;anti-Ro60 antibodies&#41; and&#47;or a focal lymphocytic infiltrate in the salivary glands&#44; forming accumulations of more than 50 lymphocytes&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Although the extraglandular involvement is what determines the prognosis&#44; it has not been included in the different classification criteria&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">An index of disease activity has been developed&#44; the <span class="elsevierStyleItalic">EULAR Sj&#246;gren</span>&#8217;<span class="elsevierStyleItalic">s syndrome disease activity index</span> &#40;ESSDAI&#41;&#44; which assesses 12 different domains &#40;glandular&#44; joint&#44; pulmonary&#44; neurological&#44; haematological&#44; etc&#46;&#41;&#46; It is defined as low-grade activity when a patient has &#60;5 points on the ESSDAI score&#44; moderate between 5 and 13 points&#44; and high-grade when 14 or more points are obtained&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">SS can affect the bronchial respiratory system with the occurrence of bronchiectasis and&#47;or with involvement of the pulmonary interstitium&#46; Interstitial involvement can develop in the form of usual interstitial pneumonia &#40;UIP&#41;&#44; non-specific interstitial pneumonia &#40;NSIP&#41; or lymphoid pneumonitis&#44; among others&#46;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> The exact incidence of SS-associated lung involvement is not known&#44;<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> although it is estimated to be present in 15&#37;&#8211;35&#37; of patients&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Respiratory symptoms related to Sj&#246;gren&#8217;s syndrome</span><p id="par0020" class="elsevierStylePara elsevierViewall">JS-related respiratory symptoms are varied&#44; very often non-specific and usually develop progressively during disease follow-up&#44; although they may be present at the time of diagnosis&#46;<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a> Clinically&#44; patients report dry cough&#44; xerotrachea and symptoms compatible with bronchial hyperresponsiveness&#46; In addition&#44; they may present with recurrent respiratory infections and dyspnoea&#46; It is not uncommon for these symptoms to precede the diagnosis of the disease and go unnoticed&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> Systematic examination of the respiratory system is therefore important&#46; The prevalence of dry cough and xerotrachea&#44; defined as the persistent sensation of dryness in the pharyngeal and retrosternal area&#44; is 40&#37;&#8211;50&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> Other less common symptoms are anosmia&#44; nasal crusts and nosebleed due to nasal dryness&#46;<a class="elsevierStyleCrossRefs" href="#bib0050"><span class="elsevierStyleSup">10&#44;11</span></a> Airway involvement may appear in the form of bronchiectasis or bronchial hyperresponsiveness and is associated with an increased frequency of respiratory infections&#46; The prevalence of bronchiectasis can be up to 10&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">The development of interstitial lung disease &#40;ILD&#41; is more common in older patients and in those with Raynaud&#8217;s phenomenon and gastrointestinal involvement in the form of motility disorder and gastroesophageal reflux&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> Its presence is not associated with specific clinical manifestations&#44; although progressive dyspnoea is its main symptom&#46;</p></span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Immunology and diagnosis of Sj&#246;gren&#8217;s syndrome</span><p id="par0030" class="elsevierStylePara elsevierViewall">As already mentioned&#44; most patients with SS are ANA positive and approximately 50&#37; are RF positive&#46; However&#44; the 2016 classification criteria for SS only include anti-Ro-60&#47;SSA antibodies&#44; which are present in 60&#37;&#8211;70&#37; of cases&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Although anti-Ro&#47;SSA antigen is known to comprise two subunits &#40;Ro60 and Ro52&#41;&#44; many laboratory techniques cannot differentiate one subunit from another&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> Anti-Ro52 antibodies are not considered diagnostic of SS&#46;<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> Therefore&#44; although in an appropriate clinical context the presence of anti-Ro52 is suggestive of SS&#44; it should be borne in mind that it is of a more non-specific nature and can be found in various systemic autoimmune diseases such as systemic lupus erythematosus&#44; scleroderma or rheumatoid arthritis&#44; where its presence is associated with Raynaud&#8217;s phenomenon and&#47;or interstitial lung disease&#46;<a class="elsevierStyleCrossRefs" href="#bib0075"><span class="elsevierStyleSup">15&#8211;18</span></a> Similarly&#44; the finding of hypergammaglobulinemia&#44; positive ANA or RF results in a patient with sicca syndrome does not allow the patient to be classified as having SS&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> Thus&#44; if positive ANA&#44; RF&#44; or anti-Ro52 results are detected&#44; a complete history-taking and physical examination should be performed to assess the possible presence of an autoimmune disease<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> and&#44; if SS is suspected&#44; a minor salivary gland biopsy should be performed to confirm the diagnosis&#46; In fact&#44; the histopathological study of the minor salivary gland is usually diagnostic in 37&#37;&#8211;50&#37; of patients with sicca syndrome&#44; ANA and&#47;or RF but negative for anti-Ro60&#47;SSA antibodies&#46;</p><p id="par0035" class="elsevierStylePara elsevierViewall">Regarding immunological findings&#44; the presence of anti-centromere antibodies &#40;ACA&#41;&#44; typically associated with scleroderma&#44; has been described in up to 20&#37; of patients with SS&#44; although it seems that these antibodies would recognize a different epitope&#46;<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> If present&#44; therefore&#44; an overlap between the two diseases must be ruled out&#44; especially if there is interstitial lung involvement&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a></p><p id="par0040" class="elsevierStylePara elsevierViewall">Diagnosis of patients with SS who do not have anti-Ro60 is often more complex&#44; as minor salivary gland biopsy is not always diagnostic&#46; Nevertheless&#44; the clinician should use all available options to achieve such a diagnosis&#44; as extraglandular complications can occur with similar severity in anti-Ro60 positive and anti-Ro60 negative patients and may be the initial manifestation of the disease&#46;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a> In these patients&#44; it is especially important to perform a minor salivary gland biopsy&#44; which would confirm the diagnosis and its classification&#44; or other tests such as parotid gland ultrasound&#44; salivary scintigraphy and a complete assessment of tear function&#44; which can reinforce the suspected diagnosis&#46;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Clinical-radiological diagnostic evaluation of lung involvement</span><p id="par0045" class="elsevierStylePara elsevierViewall">Characterization of pulmonary involvement in SS should be done in a multimodal way&#44; evaluating clinical manifestations&#44; respiratory function tests &#40;RFTs&#41; and radiological findings on chest high-resolution computed tomography &#40;HRCT&#41;&#46;</p><p id="par0050" class="elsevierStylePara elsevierViewall">Pulmonary function tests should include a complete spirometry&#44; including lung volumes with a bronchodilator test and the diffusing capacity of lung for CO test &#40;DLCO&#41;&#46; These tests will allow us to screen for the presence of airway and&#47;or parenchymal pathology&#44;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a> as well as detect significant changes that may lead to the initiation of immunosuppressive or antifibrotic treatment during disease progression&#46;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a> In addition&#44; they will allow us to rule out the possible existence of pulmonary arterial hypertension&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> Patients with SS may exhibit alterations in pulmonary function tests&#44; both obstructive and restrictive&#46; If a restrictive pattern and&#47;or a decrease in DLCO is found&#44; parenchymal or vascular involvement in the lungs should be considered&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a> In patients with obstructive lung involvement&#44; whether or not associated with restrictive compromise&#44; consideration should be given to possible airway involvement&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">Radiologically&#44; the gold standard for the study of the airway and lung parenchyma is a chest HRCT&#44; which should include an expiratory phase study to assess the presence of air trapping&#46; The most commonly observed findings are a combination of ground glass opacities&#44; consolidations&#44; honeycombing&#44; cross-linking&#44; and the occurrence of cysts&#44; nodules&#44; and bronchiectasis&#44;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a> with the NSIP pattern being the most common in terms of interstitial involvement&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> The study by Roca et al&#46;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a> found such involvement in 33&#46;3&#37; of patients&#44; followed by the UIP pattern &#40;23&#46;8&#37;&#41;&#44; lymphoid interstitial pneumonia &#40;9&#46;5&#37;&#41; and organising pneumonia &#40;9&#46;5&#37;&#41;&#46; 23&#46;8&#37; of patients had an indeterminate pattern on HRCT&#46; The possible existence of an underlying lymphoma should be assessed in any patient presenting with lymphoid interstitial pneumonia&#44; pulmonary cysts or nodules and a suggestive clinical context &#40;cytopenias&#44; C4 hypocomplementemia&#44; presence of rheumatoid factor or monoclonal gammopathy&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0170"><span class="elsevierStyleSup">34&#8211;36</span></a> It is noteworthy that&#44; unlike in scleroderma&#44; the EULAR guidelines for the management of SS do not assess the extent of interstitial involvement on chest HRCT to justify changes in treatment&#44; although symptoms and functional lung involvement do&#46;<a class="elsevierStyleCrossRefs" href="#bib0185"><span class="elsevierStyleSup">37&#44;38</span></a></p><p id="par0060" class="elsevierStylePara elsevierViewall">The prevalence of bronchiectasis in SS is not well defined&#44; with a variable proportion between 7&#37;&#8211;54&#37;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> having been reported&#46; Bronchiectasis is usually cylindrical and predominantly occurs in the lower lobes of the lungs&#46; These findings have been associated with a higher frequency of hiatal hernia and an increased risk of respiratory infections&#46;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">Consensus recommendations from <span class="elsevierStyleItalic">The Sj&#246;gren</span>&#8217;<span class="elsevierStyleItalic">s Foundation</span> &#40;USA&#41; have recently been published describing the pulmonary evaluation of patients with JS with and without known pulmonary involvement&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a> These recommendations can be differentiated according to the presence of airway and&#47;or interstitial involvement&#46; In patients without respiratory symptoms&#44; a chest X-ray and RFTs are recommended as a baseline evaluation&#46; Routine chest HRCT is not recommended&#46; Rather&#44; a chest HRCT and RFTs should be performed in patients with respiratory symptoms&#46; As there is insufficient evidence&#44; there is no established frequency for follow-up imaging or RFTs&#44; and it is recommended that follow-up be done on an individual basis&#46; Routine bronchoscopy with bronchoalveolar lavage or transbronchial biopsy is not recommended for the diagnosis of interstitial involvement&#46;</p><p id="par0070" class="elsevierStylePara elsevierViewall">Finally&#44; according to the ESSDAI index&#44; SS activity in the lungs is classified as absent&#44; mild&#44; moderate or severe&#47;intense&#44; depending on the findings in the complementary diagnostic tests and the patient&#8217;s symptoms &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Tests that define the severity of pulmonary involvement include RFTs and chest HRCT&#46; Other diagnostic tests used for respiratory evaluation include the six-minute walk test&#44; lung ultrasound&#44; or chest MRI&#46; ESSDAI considers chronic damage to be those symptoms&#44; findings on chest HRCT or RFTs&#44; which do not change over 12 months&#46;<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">38</span></a> Thus&#44; despite the abnormality in the examinations&#44; if there is no change in the previous 12 months&#44; these findings score zero on the ESSDAI index&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Pulmonary histopathology and Sj&#246;gren&#8217;s syndrome</span><p id="par0075" class="elsevierStylePara elsevierViewall">The most characteristic finding of pulmonary interstitium histology in SS is the combination of several pathological patterns&#46; The most commonly found pattern is NSIP&#44; described in up to 45&#37; of lung biopsies from patients with SS&#44; showing interstitial inflammation with varying degrees of fibrosis in a lung with preserved architecture&#46;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> The second histological pattern by frequency is UIP&#44; present in between 16&#37;&#8211;33&#37; of patients with ILD and SS&#46; Histological manifestations are characterized by honeycombing&#44; patchy fibrosis with isolated fibroblastic foci&#44; and mild interstitial inflammation along with patchy alveolar infiltrates of lymphocytes&#44; plasma cells&#44; and lymphoid follicles with germinal centres&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> Lymphoid interstitial pneumonia is characterized by a diffuse lymphoid infiltrate&#46; These lymphocytes are polyclonal and are accompanied by plasma cells&#44; occasionally forming lymphoid follicles and even germinal centres&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> The possible existence of bronchus-associated lymphoid tissue &#40;BALT&#41; lymphoma should be taken into account in patients with interstitial involvement and SS&#44; considering that this may be low-grade and the morphological findings difficult to characterize&#46;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">39</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">The study of other respiratory areas is also important&#46; Mononuclear cell infiltration of the airway has been demonstrated in the trachea&#44; bronchi and bronchioles and may affect the exocrine glands in this region&#46;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">40</span></a> In addition&#44; bronchoalveolar lavage studies have also shown a CD4&#43; T lymphocyte predominance&#44; even in asymptomatic patients&#46;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a></p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Lymphoma and lung involvement</span><p id="par0085" class="elsevierStylePara elsevierViewall">SS-associated lymphomas are usually <span class="elsevierStyleItalic">mucosa-associated lymphoid tissue</span> &#40;MALT&#41; type&#46; Radiographic findings on chest HRCT are in the form of pulmonary nodules or areas of consolidation&#44; often indistinguishable from benign processes or lymphocytic pneumonia&#46;<a class="elsevierStyleCrossRefs" href="#bib0170"><span class="elsevierStyleSup">34&#44;41</span></a> The use of PET&#47;CT in the event of a clinical suspicion can be useful for its diagnosis when the patient reports B symptoms&#44; constitutional symptoms&#44; etc&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">42</span></a> as it is non-specific&#46; The clinical and laboratory factors most commonly associated with lymphoma are parotid gland enlargement&#44; cryoglobulinaemic vasculitis&#44; leukopenia &#40;&#60;3000&#8239;cells&#47;mm<span class="elsevierStyleSup">3</span>&#41;&#44; positive La immunology and C4 hypocomplementemia&#46; It has been shown that the higher the number of risk factors&#44; the higher the positive predictive value for lymphoma&#44; so the finding of such markers should alert us to this possibility&#46;<a class="elsevierStyleCrossRefs" href="#bib0175"><span class="elsevierStyleSup">35&#44;43</span></a></p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Differential diagnosis of pulmonary involvement in Sj&#246;gren&#8217;s syndrome</span><p id="par0090" class="elsevierStylePara elsevierViewall">ILDs are a group of entities that have in common the inflammatory and fibrosing involvement of the lung parenchyma&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> Primary pulmonary diseases and interstitial diseases associated with systemic diseases have been described&#46; For this reason&#44; it is recommended that its evaluation be carried out in a multidisciplinary manner&#44; including clinicians&#44; radiologists and pathologists&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a></p><p id="par0095" class="elsevierStylePara elsevierViewall">In recent years&#44; a new entity called interstitial pneumonia with autoimmune features &#40;IPAF&#41; has been defined but&#44; in reality&#44; it should be considered as a working diagnosis and not an entity <span class="elsevierStyleItalic">per se</span>&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> A diagnosis of IPAF is considered in patients with ILD of unknown aetiology&#44; with clinical and serological findings or thoracic morphological changes suggestive of an underlying autoimmune disease&#44; but who cannot be diagnosed with any of them&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">In the case of a patient with IPAF&#44; it is important to perform a thorough history-taking and physical examination since these will allow us to classify the patient in some cases&#46; If SS is suspected&#44; a complete ophthalmological evaluation &#40;Schirmer&#8217;s test&#44; tear break-up time and corneal staining&#41; should be performed to rule out dry eye&#44; and salivary secretion should be assessed by salivary flow quantification or salivary scintigraphy&#44; and a minor salivary gland biopsy should be considered if the diagnosis of SS is still suspected but cannot be confirmed&#44; as they do not have specific anti-Ro60<a class="elsevierStyleCrossRefs" href="#bib0120"><span class="elsevierStyleSup">24&#44;25</span></a> antibodies&#46; It should be noted that sicca syndrome was not included in the definition of IPAF as it is not very specific and that anti-Ro52 and anti-Ro60<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> antibodies were not differentiated immunologically&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">Therefore&#44; it is of particular interest to consider the possibility of SS in patients with interstitial lung involvement of non-infiltrative aetiology&#44; who present associated sicca syndrome&#44; even if they do not have specific immunology&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Treatment and lung involvement in Sj&#246;gren&#8217;s syndrome</span><p id="par0110" class="elsevierStylePara elsevierViewall">Guidelines published by the <span class="elsevierStyleItalic">European League Against Rheumatism</span> &#40;EULAR&#41; in 2019 recommend multidisciplinary assessment of patients with SS&#46; These recommendations were made through the evaluation of studies published up to 2017 using a Delphi process&#44; with no evidence of significant progress in recent years&#46; Treatment is mainly based on symptomatic control of the sicca syndrome&#44; glucocorticoids and immunosuppressants&#46;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">44</span></a></p><p id="par0115" class="elsevierStylePara elsevierViewall">The consensus guidelines of <span class="elsevierStyleItalic">The Sj&#246;gren&#8217;s Foundation</span> recommend treatment according to the site of the pathology&#44; airway or pulmonary interstitium&#44; and according to the severity of symptoms&#44; severity of organ involvement and treatment progression&#46; These include symptomatic treatment&#44; glucocorticoids&#44; immunosuppressants&#44; biological therapy&#44; and antifibrotic agents&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a> Some authors have described that they use different treatments depending on the chest HRCT findings&#46;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> However&#44; although it is known that different radiological patterns are associated with different prognosis&#44; no specific treatment guidelines have been described as the current evidence is scarce&#46;<a class="elsevierStyleCrossRefs" href="#bib0025"><span class="elsevierStyleSup">5&#44;29&#44;45</span></a></p><p id="par0120" class="elsevierStylePara elsevierViewall">Regarding SS-related pulmonary involvement&#44; the 2019 EULAR guidelines recommend a treatment adjusted to the clinical findings and the ESSDAI score&#46; Inhaled therapy is recommended in patients with bronchial involvement and systemic treatment when there is ILD&#46; If involvement is moderate&#44; glucocorticoid monotherapy is recommended&#44; and if activity is high&#44; glucocorticoid treatment followed by oral immunosuppression is proposed&#46; Glucocorticoids should be used at the lowest possible dose and for the shortest possible time to avoid side effects&#46; No immunosuppressive drug is prioritised but reports in the published literature suggest the more widespread use of azathioprine&#44; mycophenolate or cyclosporine A&#46; Intravenous pulsed cyclophosphamide or rituximab<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">44</span></a> are proposed as rescue therapy&#46; Retrospective series of patients with SS or connective tissue diseases &#40;including SS&#41; have shown that azathioprine&#44; mycophenolate or rituximab are associated with improved pulmonary function tests&#44; with fewer complications than oral cyclophosphamide&#46;<a class="elsevierStyleCrossRefs" href="#bib0105"><span class="elsevierStyleSup">21&#44;46&#44;47</span></a> Rituximab has also shown encouraging results&#44; although with an increased risk of respiratory infections&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">48</span></a> Despite these findings&#44; there are no randomized clinical trials comparing these treatments&#44; so the recommendations are not robust&#46;</p><p id="par0125" class="elsevierStylePara elsevierViewall">Antifibrotic therapy has shown promising results in patients with progressive fibrosing lung diseases&#46; The <span class="elsevierStyleItalic">INBUILD</span> clinical trial demonstrated a reduction in the annual fall in forced vital capacity in such patients&#44; including 170 participants &#40;25&#46;6&#37; of the total cohort&#41; with systemic autoimmune diseases&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">49</span></a> Systemic diseases in this group included rheumatoid arthritis&#44; scleroderma&#44; Sj&#246;gren&#8217;s syndrome&#44; mixed connective tissue disease&#44; undifferentiated connective tissue disease and IPAF&#46; A <span class="elsevierStyleItalic">post-hoc</span> analysis of this cohort showed that in this subgroup of patients the effect of nintedanib was maintained&#46;<a class="elsevierStyleCrossRef" href="#bib0250"><span class="elsevierStyleSup">50</span></a> It should be noted that specific studies have not been performed in patients with SS unlike other systemic autoimmune diseases such as scleroderma&#46;<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">37</span></a></p><p id="par0130" class="elsevierStylePara elsevierViewall">If&#44; despite drug therapy&#44; there is a progression of the disease with a decline in lung function and a deterioration in quality of life&#44; patients should be evaluated by lung transplant teams&#46; There is no consensus regarding the indication for transplantation given the limited evidence available and the presence of contradictory results&#46; On the one hand&#44; a retrospective study in which patients with ILD related to connective tissue diseases were compared with patients with idiopathic pulmonary fibrosis&#44; showed that the clinical course was similar in both groups&#46; This progression was studied in relation to survival&#44; acute or chronic rejection and&#47;or existence of extrapulmonary dysfunction&#46; In this cohort&#44; patients with scleroderma were excluded&#44; but a total of 26 patients with Sj&#246;gren&#8217;s syndrome were included &#40;9&#46;5&#37; of the total cohort&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">51</span></a> On the other hand&#44; a Spanish cohort including 26 patients &#40;4 of them with SJS&#41; showed a trend towards shorter survival in patients with connective tissue disease compared to those with idiopathic pulmonary fibrosis&#46;<a class="elsevierStyleCrossRef" href="#bib0260"><span class="elsevierStyleSup">52</span></a> Thus&#44; more studies are needed to evaluate the indication for lung transplantation in the context of SS&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">The treatment protocol carried out in our center includes bronchodilator therapy for patients with predominantly obstructive airway involvement&#46; Patients with interstitial lung disease were initiated on prednisone at medium doses &#40;0&#46;5&#8239;mg&#47;kg bw&#47;day&#41;&#44; with a progressive decrease in dose to 5&#8239;mg&#47;day&#44; together with mycophenolate at progressive doses up to 720&#8239;mg&#47;12&#8239;h&#46; If the patient has bronchiectasis&#44; azathioprine &#40;1&#8722;2&#8239;mg&#47;kg bw&#47;day&#41; is prioritised over mycophenolate&#44; given the risk of respiratory infections associated with the use of this drug in this group of patients&#46; In patients with progressive lung disease despite immunosuppressive therapy&#44; treatment with rituximab is initiated&#46; Patients with progressive fibrosing ILD are started on antifibrotic therapy with nintedanib&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Conclusions</span><p id="par0140" class="elsevierStylePara elsevierViewall">Pulmonary disease in SS is an understudied entity and often underdiagnosed in routine clinical practice&#44; as it presents with non-specific symptoms&#46; In all patients diagnosed with SS&#44; the presence of respiratory symptoms should be investigated and an extensive work-up by physical examination and additional tests should be performed when there is suspicion of both interstitial and airway involvement&#46; Further studies are needed to define a specific pulmonary treatment for this disease&#44; based on the extent of the disease and co-existence with other systemic conditions&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Funding</span><p id="par0145" class="elsevierStylePara elsevierViewall">This article has been prepared without funding&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Conflict of interests</span><p id="par0150" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflicts of interest in relation to the authorship and&#47;or publication of this article&#46;</p></span></span>"
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          "titulo" => "Respiratory symptoms related to Sj&#246;gren&#8217;s syndrome"
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          "titulo" => "Immunology and diagnosis of Sj&#246;gren&#8217;s syndrome"
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          "titulo" => "Clinical-radiological diagnostic evaluation of lung involvement"
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          "titulo" => "Pulmonary histopathology and Sj&#246;gren&#8217;s syndrome"
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          "titulo" => "Lymphoma and lung involvement"
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          "titulo" => "Differential diagnosis of pulmonary involvement in Sj&#246;gren&#8217;s syndrome"
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          "titulo" => "Treatment and lung involvement in Sj&#246;gren&#8217;s syndrome"
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          "titulo" => "Conclusions"
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            0 => "Sj&#246;gren&#8217;s s&#237;ndrome"
            1 => "Intersitial lung disease"
            2 => "Sicca syndrome"
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          "titulo" => "Palabras clave"
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          "palabras" => array:3 [
            0 => "S&#237;ndrome de Sj&#246;gren"
            1 => "Enfermedad pulmonar intersticial"
            2 => "S&#237;ndrome seco"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Sj&#246;gren&#8217;s syndrome is an autoimmune disease that involves exocrine glands&#46; The most characteristic symptoms consist of the <span class="elsevierStyleItalic">sicca syndrome</span> &#40;including xerostomia and dry eye - xerophtalmia&#41;&#44; but can involve multiple organs&#46; The extraglandular involvement determines the prognosis&#46; It is tipically associated with the presence of antinuclear antibodies&#44; including Ro-60 antibodies&#46; Pulmonary involvement appears as bronchiectasis and&#47;or interstitial pneumonia&#46; Considering its high prevalence&#44; it must be ruled out in all patients with respiratory symptoms by performing pulmonary function tests and high resolution computed tomography of the chest&#46; Evaluation can be completed with a transbronchial biopsy if diagnostic doubts persist&#46; Treatment includes steroid therapy&#44; inmunosupressive or antifibrotic drugs&#44; or biological therapy&#46; In selected cases pulmonary transplantation must be considered&#46;</p></span>"
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        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">El s&#237;ndrome de Sj&#246;gren es una enfermedad autoinmune que afecta a las gl&#225;ndulas exocrinas&#46; Su sintomatolog&#237;a caracter&#237;stica es el s&#237;ndrome seco en forma de xeroftalmia y xerostom&#237;a&#44; pero puede afectar a diversos &#243;rganos o sistemas&#44; y la afectaci&#243;n extraglandular es la que condiciona el pron&#243;stico de la enfermedad&#46; T&#237;picamente se asocia con la presencia de anticuerpos antinucleares&#44; que incluyen anti-Ro-60&#46; La afectaci&#243;n pulmonar aparece en forma de bronquiectasias y&#47;o neumopat&#237;a intersticial&#46; Dada la alta prevalencia de esta complicaci&#243;n&#44; su presencia debe descartarse en todos los pacientes con s&#237;ntomas respiratorios mediante pruebas de funci&#243;n respiratoria y tomograf&#237;a computarizada de alta resoluci&#243;n tor&#225;cica&#46; Se puede completar la valoraci&#243;n mediante biopsia transbronquial en aquellos casos en que existan dudas diagn&#243;sticas&#46; El tratamiento incluye glucocorticoterapia&#44; terapia inmunosupresora o antifibr&#243;tica&#44; y terapia biol&#243;gica&#46; En caso de mala evoluci&#243;n se debe valorar el trasplante pulmonar&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Mestre-Torres J&#44; Solans-Laque R&#46; S&#237;ndrome de Sj&#246;gren y afectaci&#243;n pulmonar&#46; Med Clin &#40;Barc&#41;&#46; 2022&#59;158&#58;181&#8211;185&#46;</p>"
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          "leyenda" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">ESSDAI&#58; <span class="elsevierStyleItalic">EULAR Sj&#246;gren</span>&#8217;<span class="elsevierStyleItalic">s syndrome disease activity index</span>&#59; NYHA&#58; <span class="elsevierStyleItalic">New York Heart Association</span>&#59; RFTs&#58; respiratory function tests&#59; Chest HRCT&#58; Chest high-resolution computed tomography&#59; DLCO&#58; diffusing capacity of lung for CO&#59; FVC&#58; Forced vital capacity&#46;</p>"
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                  <table border="0" frame="\n
                  \t\t\t\t\tvoid\n
                  \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Activity level&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Description&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Without activity</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">No active lung involvement&#46;</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Mild</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Persistent cough secondary to bronchial involvement&#46;</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Pulmonary involvement should be ruled out by chest HRCT and RFTs&#46;</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">The patient cannot have dyspnoea&#46;</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Moderate</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Evidence of interstitial lung disease by chest HRCT&#46;</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">RFTs abnormalities&#58;</span> 70&#37;&#8239;<span class="elsevierStyleItalic">&#62;&#8239;DLCO&#8239;&#8805;</span>&#8239;40&#37; <span class="elsevierStyleItalic">or</span> 80&#37;&#8239;<span class="elsevierStyleItalic">&#62;&#8239;FVC&#8239;&#8805;</span>&#8239;60&#37;&#46;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
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                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">There may be dyspnoea on exertion with a NYHA functional class II&#46;</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">High</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t"><span class="elsevierStyleItalic">Evidence of interstitial lung disease with dyspnoea NYHA functional class III-IV&#46;</span>&nbsp;\t\t\t\t\t\t\n
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